The first seven months of an infant of Alouatta guariba (Humboldt) (, Atelidae): interactions and the development of behavioral patterns 1

João M. D. Miranda 2, Lucas M. Aguiar 2, Gabriela Ludwig 2, Rodrigo F. Moro-Rios 2, 3 & Fernando C. Passos 2

1 Contribution number 1564 of the Departamento de Zoologia, Universidade Federal do Paraná. 2 Laboratório de Biodiversidade, Conservação e Ecologia de Animais Silvestres, Departamento de Zoologia, Universidade Federal do Paraná. Caixa Postal 19020, 81531-980 Curitiba, Paraná, Brasil. E-mail: [email protected]; [email protected]; [email protected]; [email protected]; [email protected]. 3 Bolsista CNPq/PIBIC.

ABSTRACT. The development of the interactions of an infant with its mother and the other members of its social group plays a special role in the ethology and demography of the species, with consequences for their survive and their conservation. The objective of the present study is to investigate the development of an infant of Alouatta guariba (Humboldt, 1812) in the wild, its behavior and interactions during its first seven months of age, in a remnant of Araucaria Pine Forest in Paraná State, Brazil. Using the method of instantaneous scanning with 5 min intervals, a total of 46 hours and 15 minutes of direct observation (555 individual records) showed that the infant behavioral patterns during its first four months were characterized by high dependency, which decreased progressively until the appearance of typically juvenile behaviors during the remaining 3 months. The first records of feeding on solid food, tail functionality and allomaternal care were also recorded and discussed. This work contributes to an understanding of the ontogenetic development of a poorly known aspect of this species, and thus for a more understanding of the Alouatta Lacépède, 1799. KEY WORDS. Infancy, ontogenetic development, parental care, social behavior.

RESUMO. Os sete primeiros meses de um infante de Alouatta guariba (Humboldt) (Primatesimates, Atelidae)Atelidae): interações e desenvolvimento dos padrões comportamentais. O desenvolvimento das interações do infante primata com a mãe e demais membros do grupo social tem importância na etologia e na demografia da espécie, apresentando profundas conseqüências para sua sobrevivência e portanto, na conservação da espécie. O objetivo deste trabalho foi estudar o desenvolvimento de um infante de Alouatta guariba (Humboldt, 1812) em vida livre, seu comportamento e interações durante os sete primeiros meses de vida, em um remanescente de Floresta Ombrófila Mista, Estado do Paraná, Brasil. Através do método de varredura instantânea com intervalo de cinco minutos, um total de 46 horas e 15 minutos de observações diretas (555 registros individuais) mostraram que os padrões comportamentais do infante foram de alta dependência nos primeiros quatro meses, diminuindo progressivamente até o aparecimento dos comportamentos típicos de indivíduos juvenis durante os últimos três meses. Os primeiros registros de alimen- tação sólida, funcionalidade da cauda e registros de cuidados alomaternais também foram tomados e discutidos, contribuindo para o entendimento do desenvolvimento deste infante. PALAVRAS CHAVE. Comportamento social, cuidado parental, desenvolvimento ontogenético, infância.

The principal, longest and most intense social link among pri- ing and interacting with her, the infant learns what to eat and mates is that between mother and offspring (FEDIGAN 1982, STRIER what to fear, who to dominate and who to submit to, where to 2003). Contrary to other orders, the survivorship of walk, sleep and drink (FEDIGAN 1982). In addition, the mother the infant primate is completely dependent on the care pro- might represent a source of thermoregulation, grooming and vided by members of its social group, particularly through defense against predators and other aggressors (STRIER 2003). maternal care. Therefore, it is crucial that mothers recognize Over time, the infant progressively becomes independent of their infants as their own offspring, and that they are moti- her, acquiring important biological and psychological advan- vated to provide maternal care (MAESTRIPIERI 2001). By observ- tages, such as the familiarity with its physical and social mi-

Revista Brasileira de Zoologia 22 (4): 1191–1195, dezembro 2005 1192 J. M. D. Miranda et al. lieu. At the same time, this enables the mother additional The goal of the present study was to investigate the de- chances for mating and reproducing, providing simultaneous velopment of an infant of Alouatta guariba, subspecies A. g. increase in several facets of her inclusive fitness (RHEINGOLD & clamitans Cabrera, 1940 in the wild, as well as its maternal and ECKERMAN 1970). allomaternal relationships during the first seven months of its Starting with the pioneer work of HARLOW & ZIMMERMANN life, in a remnant of Araucaria Pine forest in Southern Brazil. (1959) on the affective links of infants of Macaca Lacépède, 1799, several studies in the field and in captivity, have addressed MATERIAL AND METHODS the behavioral interactions between mother and offspring in The present study was conducted in a 700 ha remnant of non–human primates, both in the Old and in the New World Araucaria Pine Forest located in the Bugre district, Municipal- (RHEINGOLD & ECKERMAN 1970). Therefore, special emphasis on ity of Balsa Nova, State of Paraná (25º29’52”W and 49º39’24”S). the study of this behavior are of crucial importance to under- The climate in the region is of the Cfb type according to the stand the biology, ethology and demography of these , Köpen classification (IAPAR 1978), with an average annual tem- given that, once the success of this ontogenetic phase is guar- perature of 18ºC and average annual rainfall of 1600 mm (data anteed, there is increased chance of recruitment and thus of obtained from the Meteorological Station of the Municipality group and population growth. of Lapa). Being composed mostly of altered primary forest, this In addition to maternal care, paternal investments and remnant experienced a pressure of selective tree cutting over other forms of allomaternal care might be present in several spe- its history. Currently, this region is conserved as part of the cies depending on their social systems. The quality and quan- State Area of Environmental Protection of the Devonian Scarp. tity of allomaternal interactions with infants would depend on This study was planned during the monitoring of one of the degree of kinship: when group members are closely related the groups of A. guariba that have been followed in the study (1), the interactions of this kind could be more cooperative; area since 2002 (MIRANDA & PASSOS 2004, 2005). Beginning on however, when group members are not closely related (2), ex- the birth of the infant in question (in the week between 11 pected interactions could be of a more competitive nature (CLARKE and 18 April 2004), it was possible to study its development et al. 1998). and its interactions in the wild. In April of 2004, time of the In the case of neotropical primates, polygynic systems birth of the infant, the group was composed by an adult male, such as the one found in Cebus Erxleben, 1777 and monogamic two adult females, a sub-adult male, a juvenile I and a juvenile families such as those found in callitrichids might produce the II (age/sex classification sensu MENDES 1989). During the next allomaternal interactions expected under (1) (see SÁNCHEZ et al. seven months, this infant and its mother were the main foci of 1999, SCHRADIN & ANZENBERGER 2001, TARDIFF et al. 2002). On the observation, being followed during data collection with respect other hand, in the genus Alouatta Lacépède, 1799 the social to their interactions and behavioral patterns. These data were system is shaped by male and female migrations, generating obtained using the method of instantaneous scann sampling lower relatedness, causing interactions to be expected to corre- with records every five minutes (ALTMANN 1974). spond to (2). However, few studies have addressed directly those The infant was born in the Fall of 2004, more precisely interactions in species of the genus Alouatta. In general, such in the week between 11 and 18 of April, when it was first seen descriptions are concentrated on the two most studied species: and, together with its mother and the other members of the A. seniculus (Linnaeus, 1766) and A. palliata (Gray, 1848) (LYALL group, started to be followed by the observers. The mother and 1996 and see reviews in NEVILLE et al. 1988, DEFLER 2004), in the infant were followed during the first seven months of the addition to the works by CALEGARO-MARQUES & BICCA-MARQUES infant’s life, totaling 46 hours and 15 minutes of direct obser- (1993a) on Alouatta caraya (Humboldt, 1812). vations, and 555 individual records. With regard to the investigation of infancy of individu- als of A. guariba (Humboldt, 1812), a species endemic to the RESULTS South and Southeast portions of the Brazilian Atlantic , no study has hitherto given priority to this theme During the first days of its life, the infant was positioned in such studies. Given that it is still unclear how the informa- 100% of the time ventrally of its mother, being active only tion based on the three well known species described above during nursing (Fig. 1). At the end of the first month of life, can be extrapolated to the rest of the genus Alouatta (RUMIZ the use of this position gradually started to decrease and the 1990), studies on the behavioral mother-offspring interaction dorsum of the mother was used more frequently: 60 % in the in A. guariba and other species are necessary to understand this ventral position and 30% in the dorsal position. Also follow- genus in a more holistic way. This information might also con- ing a progressive manner, peaking during its fifth month of tribute vital information for the conservation of this species, age, the infant began to behave more independently, with ex- which is currently enlisted vulnerable to extinction in several ploratory behaviors and movements away from its mother (Fig. sites along its geographical range (IBAMA 2003, MARQUES 2003, 1), which was observed, in some occasions, even to reject the MARGARIDO & BRAGA 2004). infant and to prevent it to position itself on her dorsum.

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100 During the month of April, right before completing one 80 month of age, no form of allomaternal care was observed. Start- ing in May, the infant initiated exploratory behaviors, particu- 60 larly on its mother’s body. In the same month, other individu- 40 als were recorded carrying the infant on their dorsum: a juve- nile male II, a sub-adult male and an adult female, in that or- %ofTime 20 der of occurrence. Male individuals were identified as their 0 brothers, however its relatedness with the other adult female is unknown. In the beginning of the same month, there was 01234567 the first record of consumption of solid food by the infant: age in months Venter Dorsum Independent new leaves of the “bracatinga” – Mimosa scabrella Benth., with the second and third records occurring in the beginning of Figure 1. Position of the infant in relation to the body of the mother. June and July (second and third months of age): a fruit and a N = 555 records. floral bud, respectively. In the middle of May, the first prehen- sile use of the tail was observed, when the infant was in a hang- ing posture during exploratory activities near its mother. Already during its first month the infant began to de- In June, at age of two months, the infant used the oppor- scend from the dorsum of its mother, although always remain- tunity when the mother descended to a water puddle beside a ing close to her. In the next month, the time spent by the in- creek to drink water, and, while still being on its mother’s back, fant away from its mother’s dorsum gradually increased and, leaned downward to drink directly with its mouth, supporting during the month of September, at the age of five months, it its body with one of its hands on the ground. In August, when it spent 90% of its time with no contact with her, although occa- was close to four months of age, the infant began to participate sionally climbing her back, culminating in a high level of in- in plays with its juvenile brothers that could be classified as fights dependence in the last months of the study. and chases. Starting in the same month, plays became frequent The behavioral patterns of the infant during its first four during resting periods of the adult individuals. months were closely linked and dependent on its mother, yet In September, at the age of five months, its activities starting on the fifth month, this relationship weakened and started to become more independent of its mother, including other activities such as rest, feeding on solid food and move- movement by itself. The began a transition phase and ment began to dominate its daily behaviors, which began to in November, at the age of seven months, when its behaviors appear progressively more like the independent juvenile indi- became increasingly similar to juvenile I individuals. viduals (Fig. 2). DISCUSSION The results obtained in the present study with respect to the age variation in the position of the infant in the body of its 100 mother are similar to what is observed in other species of the genus Alouatta. In general, there is a gradual shift from the 80 venter to the dorsum of the mother over the course of two to four weeks in Alouatta palliata (CARPENTER 1934, ALTMANN 1959, 60 LYALL 1996, DEFLER 2004), six to ten weeks in A. senilicus (MACK 1979, NEVILLE et al. 1988, DEFLER 2004), and even later as in the 40 case of A. belzebul (Linnaeus, 1766), where an infant was car- %ofTime ried on the venter of the mother for three months and then on 20 her back for five more months (BONVICINO 1989). Although MACK (1979) and CLARKE (1990) indicate that 0 the consumption of solid food by infants occurs from the sec- 01234567 ond month of age on, the present study observed this behav- age in months ior when the infant was only one month of age, as observed by Interaction with mother interaction with another one LYALL (1996) on A. palliata. According to MACK (1979), NEVILLE et Resting Feeding al. (1988) and DEFLER (2004), the tail of an Alouatta infant is only functional when it is one and a half to two months of Locomotion Exploration age. However, the present study indicates that the studied in- Figure 2. Development of the activity pattern of the infant along fant showed tail functionality by supporting its own weight its first seven months of life. N = 555 records. when it was only one-month-old, according with LYALL (1996)

Revista Brasileira de Zoologia 22 (4): 1191–1195, dezembro 2005 1194 J. M. D. Miranda et al. study. These small variations in infant developmental period Primatologica, Basel, 63 (4): 216-220. can occur among species, among sexes, environments, indi- BONVICINO, C.R. 1989. Ecologia e comportamento de Alouatta viduals peculiarties and even depending on the time of the belzebul (Primates: ) na Mata Atlântica. Revista year when the infant was born (FEDIGAN 1982, CLARKE 1990, Nordestina de Biologia, João Pessoa, 6 (2): 149-179. CALEGARO-MARQUES & BICCA-MARQUES 1993b, STRIER 2003, KOWALEWSKI BRAVO, S.P & A. SALLENAVE. 2003. Foraging behavior and activity & ZUNINO 2004). patterns of Alouatta caraya in the northeastern Argentinean In September, the five-month-old infant started to display Flooded Forest. International Journal of , instances of movement, feeding and participation in plays in a Chicago, 24 (4): 825-846. way similar to the patterns observed in juvenile animals CALEGARO-MARQUES, C. & J.C. BICCA-MARQUES. 1993a. Allomaternal (BONVICINO 1989, MENDES 1989, CHIARELLO 1993, BICCA-MARQUES & care in the (Alouatta caraya). Folia CALEGARO-MARQUES 1994). According to MACK (1979), these be- Primatologica, Basel, 61: 104-109. haviors can represent the beginning of their independence and CALEGARO-MARQUES, C. & J.C. BICCA-MARQUES. 1993b. Reprodu- a shift in their age class. As suggested by MENDES (1989) and used ção de Alouatta caraya Humboldt, 1812 (Primates, Cebidae), by MIRANDA & PASSOS (2005), the focal animal of this study would p. 51-66. In: M.E. YAMAMOTO & M.B.C. SOUZA (Eds). A Prima- be in a transition phase between an infant and a juvenile I. tologia no Brasil – 4. Salvador, FNMA, UFRN, Sociedade The present study recorded few instances of allomaternal Brasileira de Primatologia, 327p. care, a result consistent with a social system shaped by male CARPENTER, C.R. 1934. A field study of behavior of howling and female migrations and the ensuing decrease in relatedness monkeys. Comparative Psychology Monography, Fort among members of the group (see CLARKE et al. 1998). How- Worth, 10: 1-68. ever, allomaternal care was common in other Alouatta species CHIARELLO, A.G. 1993. Activity pattern of the such as A. palliata (CLARKE et al. 1998), A. senilicus (MACK 1979) monkey Alouatta fusca, Geoffroy 1812, in a forest fragment and A. caraya (CALEGARO-MARQUES & BICCA-MARQUES 1993a, BRAVO of southeastern Brazil. Primates, Tóquio, 34 (3): 173-175. & SALLENAVE 2003), particularly by other females of the group. CLARKE, M.R. 1990. Behavioral development and socialization However, these three species form large groups (NEVILLE et al. of infants in a free-ranging group of Howling Monkeys 1988, RUMIZ 1990, TREVES 2001, DEFLER 2004) in contrast to what (Alouatta palliata). Folia Primatologica, Basel, 54: 1-15. is observed in A. guariba (SILVA JR. 1981, NEVILLE et al. 1988, MENDES CLARKE, M.R.; K.E. GLANDER & E.L. ZUCKER. 1998. Infant-non- 1989, MIRANDA & PASSOS 2005). In the present study, males (their mother interactions of free-ranging Mantled Howlers brothers) were the most involved in interactions with the in- (Alouatta palliata) in Costa Rica. International Journal of fant, both in carrying and in plays. This was possibly a conse- Primatology, Chicago, 19 (3): 451-472. quence of their degree of relatedness of those individuals with DEFLER, T.R. 2004. Primates of Colombia. Bogotá, Conservation the infant, as well as the scarcity of females in the group (see International, 550p. Material and Methods). FEDIGAN, L.M. 1982. Primate Paradigms: sex roles and social Consistent to what was previously pointed out by RUMIZ bonds. Montreal, Eden Press, 386p. (1990), the present study indicates that data available for some HARLOW, H.F. & R.R. ZIMMERMANN. 1959. Affectional responses in species often cannot be extrapolated to others, and that addi- the infant monkey. Science, Washington, 130 (3373): 421- tional field information on parental care and infant develop- 432. ment should be obtained to fully comprehend this topic in the IAPAR. 1978. Cartas climáticas básicas do estado do Paraná. genus Alouatta. On the other hand, information obtained here Londrina, Instituto Agronômico do Paraná, 38p. already contribute to a better understanding on infants of A. g. IBAMA. 2003. Lista das espécies da fauna brasileira ameaçadas clamitans, its social interactions and its behaviors. de extinção. Brasília, Ibama, 19p. KOWALEWSKI, M. & G.E. ZUNINO. 2004. 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Received in 10.V.2005; accepted in 06.XII.2005.

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